Skip to main content
Erschienen in: Brain Topography 6/2016

12.08.2016 | Original Paper

Abnormal Complex Auditory Pattern Analysis in Schizophrenia Reflected in an Absent Missing Stimulus Mismatch Negativity

verfasst von: Dean F. Salisbury, Alexis G. McCathern

Erschienen in: Brain Topography | Ausgabe 6/2016

Einloggen, um Zugang zu erhalten

Abstract

The simple mismatch negativity (MMN) to tones deviating physically (in pitch, loudness, duration, etc.) from repeated standard tones is robustly reduced in schizophrenia. Although generally interpreted to reflect memory or cognitive processes, simple MMN likely contains some activity from non-adapted sensory cells, clouding what process is affected in schizophrenia. Research in healthy participants has demonstrated that MMN can be elicited by deviations from abstract auditory patterns and complex rules that do not cause sensory adaptation. Whether persons with schizophrenia show abnormalities in the complex MMN is unknown. Fourteen schizophrenia participants and 16 matched healthy underwent EEG recording while listening to 400 groups of 6 tones 330 ms apart, separated by 800 ms. Occasional deviant groups were missing the 4th or 6th tone (50 groups each). Healthy participants generated a robust response to a missing but expected tone. The schizophrenia group was significantly impaired in activating the missing stimulus MMN, generating no significant activity at all. Schizophrenia affects the ability of “primitive sensory intelligence” and pre-attentive perceptual mechanisms to form implicit groups in the auditory environment. Importantly, this deficit must relate to abnormalities in abstract complex pattern analysis rather than sensory problems in the disorder. The results indicate a deficit in parsing of the complex auditory scene which likely impacts negatively on successful social navigation in schizophrenia. Knowledge of the location and circuit architecture underlying the true novelty-related MMN and its pathophysiology in schizophrenia will help target future interventions.
Literatur
Zurück zum Zitat Alain C, Cortese F, Picton TW (1998a) Event-related brain activity associated with auditory pattern processing. NeuroReport 9:3537–3541CrossRefPubMed Alain C, Cortese F, Picton TW (1998a) Event-related brain activity associated with auditory pattern processing. NeuroReport 9:3537–3541CrossRefPubMed
Zurück zum Zitat Alain C, Hargrave R, Woods DL (1998b) Processing of auditory stimuli during visual attention in patients with schizophrenia. Biol Psychiatry 44:1151–1159CrossRefPubMed Alain C, Hargrave R, Woods DL (1998b) Processing of auditory stimuli during visual attention in patients with schizophrenia. Biol Psychiatry 44:1151–1159CrossRefPubMed
Zurück zum Zitat Alho K, Tervaniemi M, Huotilainen M, Lavikainen J, Tiitinen H, Ilmoniemi RJ, Knuutila J, Näätänen R (1996) Processing of complex sounds in the human auditory cortex as revealed by magnetic brain responses. Psychophysiology 33:369–375CrossRefPubMed Alho K, Tervaniemi M, Huotilainen M, Lavikainen J, Tiitinen H, Ilmoniemi RJ, Knuutila J, Näätänen R (1996) Processing of complex sounds in the human auditory cortex as revealed by magnetic brain responses. Psychophysiology 33:369–375CrossRefPubMed
Zurück zum Zitat Erickson MA, Ruffle A, Gold JM (2016) A meta-analysis of mismatch negativity in schizophrenia: from clinical risk to disease specificity and progression. Biol Psychiatry 79:980–987CrossRefPubMed Erickson MA, Ruffle A, Gold JM (2016) A meta-analysis of mismatch negativity in schizophrenia: from clinical risk to disease specificity and progression. Biol Psychiatry 79:980–987CrossRefPubMed
Zurück zum Zitat Fishman Y, Steinschneider M (2012) Searching for the mismatch negativity in primary auditory cortex of the awake monkey: deviance detection or stimulus specific adaptation? J Neurosci 32:15747–15758CrossRefPubMedPubMedCentral Fishman Y, Steinschneider M (2012) Searching for the mismatch negativity in primary auditory cortex of the awake monkey: deviance detection or stimulus specific adaptation? J Neurosci 32:15747–15758CrossRefPubMedPubMedCentral
Zurück zum Zitat Ford JM, Hillyard SA (1981) Event-related potentials (ERPs) to interruptions of a steady rhythm. Psychophysiology 18:322–330CrossRefPubMed Ford JM, Hillyard SA (1981) Event-related potentials (ERPs) to interruptions of a steady rhythm. Psychophysiology 18:322–330CrossRefPubMed
Zurück zum Zitat Hirayasu Y, Shenton ME, Salisbury DF, Dickey CC, Fischer IA, Mazzoni P, Kisler T, Arakaki H, Kwon JS, Anderson JA, Yurgelun-Todd D, Tohen M, McCarley RW (1998) Lower left temporal lobe MRI volumes in patients with first-episode schizophrenia compared with psychotic patients with first-episode affective disorder and normal subjects. Am J Psychiatry 155:1384–1391CrossRefPubMed Hirayasu Y, Shenton ME, Salisbury DF, Dickey CC, Fischer IA, Mazzoni P, Kisler T, Arakaki H, Kwon JS, Anderson JA, Yurgelun-Todd D, Tohen M, McCarley RW (1998) Lower left temporal lobe MRI volumes in patients with first-episode schizophrenia compared with psychotic patients with first-episode affective disorder and normal subjects. Am J Psychiatry 155:1384–1391CrossRefPubMed
Zurück zum Zitat Jacobsen T, Schröger E (2001) Is there pre-attentive memory-based comparison of pitch? Psychophysiology 38:723–727CrossRefPubMed Jacobsen T, Schröger E (2001) Is there pre-attentive memory-based comparison of pitch? Psychophysiology 38:723–727CrossRefPubMed
Zurück zum Zitat Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC (1996) Role of cortical N-methyl D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci USA 93:11962–11967CrossRefPubMedPubMedCentral Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC (1996) Role of cortical N-methyl D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci USA 93:11962–11967CrossRefPubMedPubMedCentral
Zurück zum Zitat Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Onitsuka T, Spencer M, Yurgelun-Todd DA, Kikinis R, Jolesz FA, McCarley RW (2003) Progressive decrease of left Heschl’s gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 60:765–766 Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Onitsuka T, Spencer M, Yurgelun-Todd DA, Kikinis R, Jolesz FA, McCarley RW (2003) Progressive decrease of left Heschl’s gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 60:765–766
Zurück zum Zitat Konopaske GT, Sweet RA, Wuc Q, Sampson A, Lewis DA (2006) Regional specificity of chandelier neuron axon terminal alterations in schizophrenia. Neuroscience 138:189–196CrossRefPubMed Konopaske GT, Sweet RA, Wuc Q, Sampson A, Lewis DA (2006) Regional specificity of chandelier neuron axon terminal alterations in schizophrenia. Neuroscience 138:189–196CrossRefPubMed
Zurück zum Zitat Korzyukov OA, Winkler I, Gumenyuk VI, Alho K (2003) Processing abstract auditory features in the human auditory cortex. NeuroImage 20:2245–2258CrossRefPubMed Korzyukov OA, Winkler I, Gumenyuk VI, Alho K (2003) Processing abstract auditory features in the human auditory cortex. NeuroImage 20:2245–2258CrossRefPubMed
Zurück zum Zitat Lewis DA, Sweet RA (2009) Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. J Clin Investig 119:706–716CrossRefPubMedPubMedCentral Lewis DA, Sweet RA (2009) Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. J Clin Investig 119:706–716CrossRefPubMedPubMedCentral
Zurück zum Zitat Maess B, Jacobsen T, Schröger E, Friederici AD (2007) Localizing pre-attentive auditory memory-based comparison: magnetic mismatch negativity to pitch change. NeuroImage 37:561–571CrossRefPubMed Maess B, Jacobsen T, Schröger E, Friederici AD (2007) Localizing pre-attentive auditory memory-based comparison: magnetic mismatch negativity to pitch change. NeuroImage 37:561–571CrossRefPubMed
Zurück zum Zitat May PJC, Tiitinen H (2010) Mismatch negativity (MMN), the deviance-elicited auditory deflection, explained. Psychophysiology 47:66–122CrossRefPubMed May PJC, Tiitinen H (2010) Mismatch negativity (MMN), the deviance-elicited auditory deflection, explained. Psychophysiology 47:66–122CrossRefPubMed
Zurück zum Zitat Michie PT (2001) What has MMN revealed about the auditory system in schizophrenia? Int J Psychophysiol 42:177–194CrossRefPubMed Michie PT (2001) What has MMN revealed about the auditory system in schizophrenia? Int J Psychophysiol 42:177–194CrossRefPubMed
Zurück zum Zitat Näätänen R (1990) The role of attention in auditory information processing as revealed by event-related potentials and other measures of cognitive function. Behav Brain Sci 13:201–288CrossRef Näätänen R (1990) The role of attention in auditory information processing as revealed by event-related potentials and other measures of cognitive function. Behav Brain Sci 13:201–288CrossRef
Zurück zum Zitat Näätänen R, Kujala T, Escera C, Baldeweg T, Kreegipuu K, Carlson S, Ponton C (2012) The mismatch negativity (MMN). A unique window to disturbed central auditory processing in ageing and different clinical conditions. Clin Neurophysiol 123:424–458CrossRefPubMed Näätänen R, Kujala T, Escera C, Baldeweg T, Kreegipuu K, Carlson S, Ponton C (2012) The mismatch negativity (MMN). A unique window to disturbed central auditory processing in ageing and different clinical conditions. Clin Neurophysiol 123:424–458CrossRefPubMed
Zurück zum Zitat Näätänen R, Sussman ES, Salisbury DF, Shafer VL (2014) Mismatch negativity (MMN) as an index of cognitive dysfunction. Brain Topogr 27:451–466CrossRefPubMedPubMedCentral Näätänen R, Sussman ES, Salisbury DF, Shafer VL (2014) Mismatch negativity (MMN) as an index of cognitive dysfunction. Brain Topogr 27:451–466CrossRefPubMedPubMedCentral
Zurück zum Zitat Nordby H, Roth WT, Pfefferbaum A (1988) Event-related potentials to breaks in sequences of alternating pitches or interstimulus intervals. Psychophysiology 25:262–268CrossRefPubMed Nordby H, Roth WT, Pfefferbaum A (1988) Event-related potentials to breaks in sequences of alternating pitches or interstimulus intervals. Psychophysiology 25:262–268CrossRefPubMed
Zurück zum Zitat Saarinen J, Paavilainen P, Schröger E, Tervaniemi M, Näätänen R (1992) Representation of abstract attributes of auditory stimuli in the human brain. NeuroReport 3:1149–1151CrossRefPubMed Saarinen J, Paavilainen P, Schröger E, Tervaniemi M, Näätänen R (1992) Representation of abstract attributes of auditory stimuli in the human brain. NeuroReport 3:1149–1151CrossRefPubMed
Zurück zum Zitat Salisbury DF (2012) Finding the missing stimulus mismatch negativity: emitted MMN to violations of an auditory gestalt. Psychophysiology 49:544–548CrossRefPubMedPubMedCentral Salisbury DF (2012) Finding the missing stimulus mismatch negativity: emitted MMN to violations of an auditory gestalt. Psychophysiology 49:544–548CrossRefPubMedPubMedCentral
Zurück zum Zitat Salisbury DF, Shenton ME, Griggs CB, Bonner-Jackson A, McCarley RW (2002) Mismatch negativity in chronic schizophrenia and first-episode schizophrenia. Arch Gen Psychiatry 59:686–694CrossRefPubMed Salisbury DF, Shenton ME, Griggs CB, Bonner-Jackson A, McCarley RW (2002) Mismatch negativity in chronic schizophrenia and first-episode schizophrenia. Arch Gen Psychiatry 59:686–694CrossRefPubMed
Zurück zum Zitat Salisbury DF, Kasai K, Kuroki N, Shenton ME, McCarley RW (2007) Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia. Arch Gen Psychiatry 64:521–529CrossRefPubMedPubMedCentral Salisbury DF, Kasai K, Kuroki N, Shenton ME, McCarley RW (2007) Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia. Arch Gen Psychiatry 64:521–529CrossRefPubMedPubMedCentral
Zurück zum Zitat Salisbury DF, Collins KC, McCarley RW (2010) Reductions in the N1 and P2 auditory event-related potentials in first-hospitalized and chronic schizophrenia. Schizophr Bull 36:991–1000CrossRefPubMed Salisbury DF, Collins KC, McCarley RW (2010) Reductions in the N1 and P2 auditory event-related potentials in first-hospitalized and chronic schizophrenia. Schizophr Bull 36:991–1000CrossRefPubMed
Zurück zum Zitat Salisbury DF, Polizzotto NR, Nestor PG, Haigh SM, Koehler J, McCarley RW (2016) Pitch and duration mismatch negativity and premorbid intellect in the first hospitalized schizophrenia spectrum. Schizophr Bull. doi:10.1093/schbul/sbw074 Salisbury DF, Polizzotto NR, Nestor PG, Haigh SM, Koehler J, McCarley RW (2016) Pitch and duration mismatch negativity and premorbid intellect in the first hospitalized schizophrenia spectrum. Schizophr Bull. doi:10.​1093/​schbul/​sbw074
Zurück zum Zitat Sams M, Paavilainen P, Alho K, Näätänen R (1985) Auditory frequency discrimination and event-related potentials. Electroencephalogr Clin Neurophysiol 62:437–448CrossRefPubMed Sams M, Paavilainen P, Alho K, Näätänen R (1985) Auditory frequency discrimination and event-related potentials. Electroencephalogr Clin Neurophysiol 62:437–448CrossRefPubMed
Zurück zum Zitat Schröger E, Näätänen R, Paavilainen P (1992) Event-related potentials reveal how non-attended complex sound patterns are represented by the human brain. Neurosci Lett 146:183–186CrossRefPubMed Schröger E, Näätänen R, Paavilainen P (1992) Event-related potentials reveal how non-attended complex sound patterns are represented by the human brain. Neurosci Lett 146:183–186CrossRefPubMed
Zurück zum Zitat Sculthorpe LD, Ouellet DR, Campbell KB (2009) MMN elicitation during natural sleep to violations of an auditory pattern. Brain Res 1290:52–62CrossRefPubMed Sculthorpe LD, Ouellet DR, Campbell KB (2009) MMN elicitation during natural sleep to violations of an auditory pattern. Brain Res 1290:52–62CrossRefPubMed
Zurück zum Zitat Sweet RA, Henteleff RA, Zhang W, Sampson AR, Lewis DA (2009) Reduced dendritic spine density in auditory cortex of subjects with schizophrenia. Neuropsychopharmacology 34:374–389CrossRefPubMed Sweet RA, Henteleff RA, Zhang W, Sampson AR, Lewis DA (2009) Reduced dendritic spine density in auditory cortex of subjects with schizophrenia. Neuropsychopharmacology 34:374–389CrossRefPubMed
Zurück zum Zitat Tervaniemi M, Saarinen J, Paavilainen P, Danilova N, Näätänen R (1994) Temporal integration of auditory information in sensory memory as reflected by the mismatch negativity. Biol Psychol 38:157–167CrossRefPubMed Tervaniemi M, Saarinen J, Paavilainen P, Danilova N, Näätänen R (1994) Temporal integration of auditory information in sensory memory as reflected by the mismatch negativity. Biol Psychol 38:157–167CrossRefPubMed
Zurück zum Zitat Todd J, Michie PT, Schall U, Karayanidis F, Yabe H, Näätänen R (2008) Deviant matters: duration, frequency, and intensity deviants reveal different patterns of mismatch negativity reduction in early and late schizophrenia. Biol Psychiatry 63:58–64CrossRefPubMed Todd J, Michie PT, Schall U, Karayanidis F, Yabe H, Näätänen R (2008) Deviant matters: duration, frequency, and intensity deviants reveal different patterns of mismatch negativity reduction in early and late schizophrenia. Biol Psychiatry 63:58–64CrossRefPubMed
Zurück zum Zitat Todd J, Whitson L, Smith E, Michie PT, Schall U, Ward PB (2014) What’s intact and what’s not within the mismatch negativity system in schizophrenia. Psychophysiology 51:337–347CrossRefPubMed Todd J, Whitson L, Smith E, Michie PT, Schall U, Ward PB (2014) What’s intact and what’s not within the mismatch negativity system in schizophrenia. Psychophysiology 51:337–347CrossRefPubMed
Zurück zum Zitat Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6:391–398CrossRefPubMed Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6:391–398CrossRefPubMed
Zurück zum Zitat Umbricht D, Krljes S (2005) Mismatch negativity in schizophrenia: a meta-analysis. Schizophr Res 76:1–23CrossRefPubMed Umbricht D, Krljes S (2005) Mismatch negativity in schizophrenia: a meta-analysis. Schizophr Res 76:1–23CrossRefPubMed
Zurück zum Zitat Winkler I (2007) Interpreting the mismatch negativity. J Psychophysiol 21:147–163CrossRef Winkler I (2007) Interpreting the mismatch negativity. J Psychophysiol 21:147–163CrossRef
Zurück zum Zitat Winkler I, Denham SL, Nelken I (2009) Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cognit Sci 13:532–540CrossRef Winkler I, Denham SL, Nelken I (2009) Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cognit Sci 13:532–540CrossRef
Zurück zum Zitat Yabe H, Tervaniemi M, Reinikainen K, Näätänen R (1997) Temporal window of integration revealed by MMN to sound omission. NeuroReport 8:1971–1974CrossRefPubMed Yabe H, Tervaniemi M, Reinikainen K, Näätänen R (1997) Temporal window of integration revealed by MMN to sound omission. NeuroReport 8:1971–1974CrossRefPubMed
Metadaten
Titel
Abnormal Complex Auditory Pattern Analysis in Schizophrenia Reflected in an Absent Missing Stimulus Mismatch Negativity
verfasst von
Dean F. Salisbury
Alexis G. McCathern
Publikationsdatum
12.08.2016
Verlag
Springer US
Erschienen in
Brain Topography / Ausgabe 6/2016
Print ISSN: 0896-0267
Elektronische ISSN: 1573-6792
DOI
https://doi.org/10.1007/s10548-016-0514-2

Weitere Artikel der Ausgabe 6/2016

Brain Topography 6/2016 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.